The Influence of Fallopian Tube Length on Fertility in the Rabbit*

FERTILITY AND STERILITY Copyright

©

Vol. 31, No.6, June 1979 Printed in U.s A.

1979 The American Fertility Society

THE INFLUENCE OF FALLOPIAN TUBE LENGTH ON FERTILITY IN THE RABBI'J'l'

PETER McCOMB, M.B., B.S., D.OBSTET.R.C.O.G. VICTOR GOMEL, M.D., F.R.C.S.(C)t Department of Obstetrics and Gynaecology, University of British Columbia Vancouver General Hospital, Vancouver, British Columbia, Canada V5Z IM9

The correlation between the length of the oviduct and degree of fertility was studied in 16 New Zealand White rabbits subjected to microsurgical resection of differing lengths of fallopian tube involving the isthmus in each case. A highly significant (P < 0.005) linear correlation was found, suggesting that more than 47% of an oviduct must remain distally before fertility can be anticipated. Absence of the isthmic segment of the fallopian tube was found to be associated with supracervical fetal implantations in the uterus. The importance of the assessment of tubal length as a prelude to reconstructive surgery, especially for reversal of sterilization, is emphasized. Fertil Steril31:673, 1979

Fertility subsequent to tubal reconstruction is largely dependent on the length and functional quality of the oviduct. There is a paucity of data equating the length of oviduct with the degree of fertility. Iatrogenic and pathologic lesions of the human adnexa are rarely symmetrical. It is therefore difficult, after surgical reconstruction, to attribute subsequent pregnancy to a particular length of tube, unless there is only one potentially functional oviduct remaining. Confounding influences such as the vast variation in tubal quality and techniques of reconstruction, and the myriad of often associated subfertility factors make the standardization of human data extremely difficult. It is important, however, to establish the critical length of tube needed for fertility so as to avoid unnecessary surgery. We have used the rabbit as our experimental model. This animal lends itself to such experimentation since it possesses a duplex genital tract to the level ofthe two cervices. Thus, each animal can serve as its own control. Furthermore, the techReceived November 7, 1978; revised January 9, 1979; accepted January 11, 1979. *Supported by Grant 1977-6 from the British Columbia Medical Research Foundation. tReprint requests: Victor Gomel, M.D., Department of Obstetrics and Gynaecology. Vancouver General Hospital, Vancouver, B. C., Canada V5Z 1M9.

673

niques of microsurgical manipulation of the rabbit oviduct have been established. I, 2 MATERIALS AND METHODS

Sixteen sexually mature New Zealand White does were included in this series. Preoperatively, the animals were individually caged, subjected to alternating 12-hour periods oflight and dark, and received a standard amount of rabbit chow and liberal water. Each rabbit was anesthetized with intravenous pentobarbitone, the abdomen was depilated, and the genital tract was displayed through a ventral midline laparotomy. Fully sterile microsurgical techniques were observed, including tissue irrigation, meticulous hemostasis, and gentle tissue handling. 3 The OPMI 6 Carl Zeiss floor-mounted microscope allowed magnification from x3.5 to x40. The length of each intact oviduct was measured with sterile paper tape. In each rabbit, the left oviduct was subjected to segmental resection and anastomosis (Fig. 1). The right oviduct was anastomosed after simple transection and served as a control. The left utero-isthmic junction was identified and preserved. The most proximal isthmus was transected with Castro-Viejo-Vannas miniature microscissors, a tubal microc1amp or fine elastic

674

MCCOMB AND GOMEL

~~i~ ~1 J

Uterine horn

!~1 : :

UTJ

a

2

Fimbriae

FIG. 1. Microsurgical resection of the rabbit oviduct. UTJ, Uterotubal junction; a, site of proximal transection; bl> b2 , sites of distal transection; arrows demonstrate varying lengths of fallopian tube excised.

thread steadying the proximal portion. Major tubal vessels were carefully preserved, and only those supplying the segment of fallopian tube to be excised were coagulated with a microelectrode or were under-run with 11-0 nylon. A microclamp or fine elastic cord was next positioned distal to the segment to be excised. The tube was transected distally with the microscissors. A microelectrode was then used to excise the intervening segment of oviduct from the mesosalpinx by electrosurgery. The excised segment of fallopian tube was measured in the limp, wet state. The mesosalpinx was reconstructed using interrupted 10-0 nylon suture material. This first step enabled a tubal anastomosis without tension. In those instances where a large proportion of fallopian tube had been excised, discrepancy existed between the diameters of the remaining tubal segments requiring anastomosis. Here the proximal tubal stump was incised for 0.5 mm along the antemesenteric border. Anastomosis was then accomplished with interrupted mucosa-sparing sutures of 11-0 nylon swaged on a 50-,..an diameter, 4 mm shroud 3/8 circle taper needle. A two-layer anastomosis of muscularis and serosa was possible in most instances. However, in some resections involving the ampulla, anastomosis could only be

June 1979

carried out in a single layer. When this was the case a few additional sutures were placed in the serosa alone to complete the anastomosis. The anastomosis was next tested by saline perfusion from a fine intracath introduced into the distal ampulla. The left tube was always transected immediately distal to the uterotubal junction. Starting at this point the excised segments varied between 4% and 67% (0.4 and 8.7 cm) of the total lengths of the oviducts (ranging from 8 cm to 13.5 cm, averaging 10.9 cm). In the doe the isthmus accounts for approximately 37% ofthe total length of the oviduct. The right oviduct was transected and anastomosed (without resection) using an identical twolayer technique. The peritoneal cavity was then lavaged with Ringer's lactate solution and the abdominal wound was closed in two layers. Prolene (2-0) was used to approximate the peritoneum and muscle layer, followed by subcuticular catgut and metal clips to the skin. After a minimum of 2 weeks' convalescence, breeding was initiated with a single fertile buck. Spontaneous copulation and thus ovulation allowed simulation of normal reproduction. Ovulation was not induced artificially so as to maintain the physiologic ratio between left and right implantation numbers. Pregnancy was diagnosed by abdominal palpation; the rabbit was then killed to determine the side of pregnancy and the state of the adnexa. Pro uterine perfusion with dilute methylene blue under magnification allowed classification ofthe anastomotic lumina as follows: N, normal; +, slightly impaired; ++, minimally patent; and + + +, occluded. The adnexal status was critically assessed microscopically and graded as follows: N, investment

TABLE 1. Results from All Rabbits Pregnancies through Transected oviduct

Resected oviduct

Fraction of resected oviduct remaining distally

5 0 6 3 3 8 6 0 4 3 9 7 6 7 5 3

2 0 6 0 3 1 0 0 0 1 0 0 0 0 0 0

0.76 0.70 0.82 0.60 0.96 0.55 0.60 0.94 0.40 0.60 0.86 0.40 0.69 0.42 0.33 0.63

Rabbit

1 2 3 4 5 6 7 8 9 10 11

12 13 14 15 16

Anatomical distortion

Patency Transected oviduct

Resected oviduct

Transected oviduct

Resected oviduct

+ +++

+++

N

N

+++

+++

N N N N N N N N N N N N N N

N N N N

+ N N N

N

N

+

++

N

N

+

+ +++

N N

+ N

+++

+

N N

N N

++

++ +

N N

N

N

N

+ + + ++ ++ ++ N

+

INFLUENCE OF FALLOPIAN TUBE LENGTH ON FERTIUTY

Vol. 31, No.6

675

TABLE 2. Results from Anatomically Pristine Animals Pregnancies through Rabbit

•

Resected oviduct

Fraction of resected oviduct remaining distally

~d~~~/~~!n:~t:~~:~~~l~~

5 6 3 8 0 4 3 5 3

2 6 3 1 0 0 1 0 0

0.76 0.82 0.96 0.55 0.94 0.40 0.60 0.33 0.63

0.4 1 1 0.125

1 3 5 6 8 9 10 15 16

I r

Transected oviduct

with mesosalpingeal fat; +, adhesions or anatomical distortion distant to the adnexum; + +, mild adhesions or anatomical distortion of the adnexal anatomy; and + + +, severe adhesions or anatomical distortion of the adnexal anatomy. The length of each oviduct was measured in the wet, limp state. RESULTS

The results are shown in Table 1. Pregnancies occurred 38 to 172 days after the surgery. Only perfect, albeit modified, adnexal anatomy was accepted since even minor distortion may influence fertility. Grade N was accepted for the anastomosis, and grade + for the adnexal status. Table 2 lists the remaining anatomically pristine animals. Of these, another rabbit was excluded since lack of pregnancy on the side ofthe surgical control oviduct, together with this animal's rejection of the buck, were suggestive of pseudocyesis. Figure 2 synthesizes the data. The correlation between the ratio of experimental to control pregnancies and the fraction of oviduct remaining distally was pronounced (r = 0.77, using Kendall's

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r = 0.77 slope = 0.43 intercept = 0.47

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correlation coefficient). This correlation was significant to P < 0.005, suggesting that 47% or more of the fallopian tube must remain distally before fertility can be anticipated. We further observed that in those cases in which the resected segment of tube was relatively small (between 4% and 18% of the total tubal length) the fetuses were spaced normally within the uterus, whereas in rabbits in which the resected segment was large (between 40% and 46% of the total length of the oviduct), the pregnancies were invariably in the proximal supracervical region of the uterus. That the greatly shortened fallopian tube (with the isthmus totally excised) permits only proximal, if any, implantation of the blastocyst suggests that the physiologic pause of the fertilized ovum within the oviduct may be crucial to its subsequent successful nidation within the uterus. DISCUSSION

The linear relationship demonstrated between oviductal length and the subsequent rate of fertility indicates that this is an important factor to consider when contemplating reconstructive surgery, especially for reversal of sterilization. In this experimental model the excision was always started immediately distal to the uterotubal junction (which was preserved) and involved the isthmus in each case. We are presently planning an experiment in which the isthmus will be conserved and differing lengths of ampulla will be excised. Until sufficient data are accumulated to allow correlation oftuballength with the occurrence of pregnancy in the human, such animal data may serve only as a useful precursor.

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0.4

0.8

1.0

Remaining Distal Fraction of Oviduct

FIG. 2. Correlation between fertility and remaining distal fraction of the oviduct.

Acknowledgments. Materials were generously supplied by Ethicon and Valley-Lab. The statistical analysis was kindly performed by B. J. Morrison, Ph.D., of the Department of Health Care and Epidemiology, University of British Columbia.

MCCOMB AND GOMEL

676 REFERENCES

1. Eddy CA, Hoffman JJ, Pauerstein CJ: Pregnancy following

segmental isthmic reversal of the rabbit oviduct. Experientia 32:1194, 1976 2. McComb P, Gomel V: The effect of segmental ampullary

June 1979

reversal on the subsequent fertility of the rabbit. Fertil Steril 31:83, 1979 3. Gomel V, McComb P: Microsurgery in gynecology. In Microsurgery, Edited by S Silber. Baltimore, Williams & Wilkins Co. In press